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Culture Systems Influence the Physiological Performance of the Soft Coral Sarcophyton Glaucum

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Culture Systems Influence the Physiological Performance of the Soft Coral Sarcophyton Glaucum www.nature.com/scientificreports OPEN Sarcophyton glaucum * Sarcophyton glaucum Certain sof corals and all reef-building corals form associations (collectively termed “holobionts”) with symbiotic dinofagellates and bacteria; these microbes are critical to the physiological function and survival of their animal hosts1−3. Although the mutualistic dinofagellates translocate photosynthetically fxed carbon into host cytoplasm, corals and other endosymbiotic anthozoans nevertheless rely on heterotrophy, as well, for nourishment 4−5. Tese mutualistic associations consequently span a bridge between benthic and planktonic food webs and consequently play critical roles as primary and secondary producers6. Te culture of alcyonacean sof corals (Cnidaria: Anthozoa: Octocorallia: Alcyonacea)- notably Sarcophyton, Sinularia, and Lobophyton- has advanced rapidly in recent decades given the needs to (1) explore the impacts of environmental change on their physiological performance and (2) develop a sustainable supply for both the marine cosmeceutical and aquarium trade industries1,7,8. Many cultured sof corals used in natural product research rely on natural seawater fow-through systems (FTS)9,10; however, natural product yields may difer from those of wild populations11. Other studies have used recirculating aquaculture systems (RAS) in which seawater quality parameters can be readily and automatically modulated by a variety of microprocessor-based dosing systems12−14. While biological factors, such as “live rocks” (typically dead coral skeleton encrusted by crustose coralline algae) that accumulate rich microbial fora15,16 and heterotrophic feeding4−5,17, have been explored more recently, a systemic comparison across diferent types of culture systems has not yet been achieved for sof corals. Light intensity and fow velocity have been examined in numerous sof coral experiments 7,17−19. Te former is especially important for sof corals harboring dinofagellates, whose photosynthetic performance can directly or indirectly afect the physiology and growth of their hosts 20,21. Light has also been shown to afect not only growth, but also secondary metabolite production, in symbiotic sof corals 19. With respect to fow, sof corals National Museum of Atlantic Oceanographic and Meteorological Laboratory, Cooperative Institute for Marine and *email: [email protected] | (2020) 10:20200 | www.nature.com/scientificreports/ Figure 1. Schematic of experimental design alongside key fndings. An image of sof corals mounted to ceramic pedestals and the tank system (A). Representative pedestals and sof coral fragments have been shown from the RAS−B (B), RAS+B (C), and FTS (D). alter their morphologies in response to changes in seawater velocity18, and seawater fow promotes material exchange and metabolism (thereby afecting metabolite yield). However, only single-factor experiments have been conducted with sof corals, despite the well-documented interaction between irradiance and water fow in hard corals like Galaxea fascicularis22. Tus, research focused on the interaction of light and fow on sof coral physiology is needed. Measurements of morphology and growth in sof corals are more difcult compared to stony corals23; the latter consist of a large amount of calcium carbonate (exoskeleton) covered by a thin veneer of live tissue. Alcyonacean sof corals, in contrast, are mostly feshy, with only small amounts of calcium carbonate (sclerite) skeleton. Shape is instead maintained by hydrostatic pressure from water pumped into a canal system. Such hydroskeletons change quickly in size and shape in response to environmental shifs. Terefore, it is difcult to accurately measure their size and growth23, though oral disc diameter (ODD), stalk diameter, colony height, and wet and dry colony weight have all been assessed in prior works 24,25. In general, ash weight and ash-free dry weight (AFDW) are thought to represent skeleton and organic matter content, respectively 25. Sof corals of the genus Sarcophyton are abundant on many coral reefs in the Indo-Pacifc Ocean, and par- ticularly Taiwan 6. Sarcophyton colonies are mushroom-shaped, with (1) feshy stalks elevating the polyp-bearing oral discs and (2) sclerites in the interior feshy tissues of the colony. Sarcophyton glaucum (Quoy & Gaimard, 1833) is a suspension feeder that lives in mutualistic association with phototrophic dinofagellates (family Sym- biodiniaceae), as well as an array of other microbes. It has been cultured in FTS to investigate natural product production9 and in RAS to assess the efects of light intensity and fow velocity on its physiology17,20,26,27. Given the recent recommendation to develop the capacity to biobank and biopreserve corals ex situ 28, a rigorous com- parison of sof coral performance across diferent culture systems is of need. Herein we aimed to study the efect of three diferent types of culture systems—a RAS with no microbial fora or exogenously supplied food [RAS minus (−) additional biological input = RAS−B], a RAS without a protein skimmer supplemented with live rocks and a supplemental phytoplankton solution fed corals [RAS plus ( +) additional biological input = RAS+B], and a traditional FTS- on the physiological performance of S. glaucum (Fig. 1). Within each culture system, two levels of photosynthetically active radiation (PAR; 100 or 200 μmol quanta m−2 s−1) and fow velocity (5 or 15 cm s−1) were administered, and several coral physiological response variables were measured to assess performance: colony color, height, base diameter, growth rate, ODD, and percent (%) organic weight (i.e., AFDW). We hypothesized that the physiological performance of the corals would be superior in the RAS+B system due to the (1) potential for heterotrophy and (2) the fact that feeding was carried out in separate feeding tanks (which would potentially limit macroalgal growth in the culture tanks). Te pH, concentrations of Ca2+and Mg2+, and carbonate hardness/alkalinity (KH) were sig- nifcantly higher in RAS−B and RAS+B than in FTS (Table 1). Levels of ammonia, nitrite, nitrate, and phosphate in the three systems remained below detectable levels (< 0.2 mg L−1) during the entire experimental period (data | (2020) 10:20200 | Vol:.(1234567890) www.nature.com/scientificreports/ Culture system Temperature (°C ) Salinity pH Ca2+ (mg L−1) Mg2+ (mg L−1) KH (dKH) RAS−B 25.7 ± 0.10B 34.8 ± 0.10 8.15 ± 0.03A 450 ± 4.80A 1318 ± 6.32AB 7.4 ± 0.15A RAS+B 26.0 ± 0.11B 34.9 ± 0.10 8.11 ± 0.03AB 447 ± 5.27A 1320 ± 5.00A 7.3 ± 0.17A FTS 26.5 ± 0.08A 35.0 ± 0.10 8.03 ± 0.02B 411 ± 4.55B 1297 ± 4.41B 7.0 ± 0.13B Table 1. Comparison of seawater chemistry parameters across the three culture systems: RAS−B (n = 13 measurements), RAS+B (n = 9), and FTS (n = 9). When the non-parametric ANOVAs detected diferences across the culture systems, Dunn’s multiple comparisons tests were carried out between individual means, and signifcant diferences (p < 0.05) are denoted by capital letters. All error terms represent standard error of the mean. Figure 2. Violin plots depicting temporal variation in buoyant weight (A), oral disc diameter (ODD: B), and fragment color (C) of sof corals over time in the three culture systems—recirculating aquarium system (RAS) without additional biological input (RAS−B; red), RAS with exogenous food supply and “live” rocks (RAS+B; green), and a fow-through system (FTS) featuring partially fltered seawater (blue)—as well as interaction plots of raw color data (D). It should be re-emphasized that RAS−B tanks were converted to RAS+B ones afer day-84. Error bars spanning mean values at each sampling time represent standard error, asterisks in (D) denote Tukey’s honestly signifcant diferences (p < 0.05) between RAS+B and FTS corals, and lowercase letters in (D) denote temporal diferences (Tukey’s HSD, p < 0.05) in color for corals of the RAS−B culture system. RAS+B vs. FTS diferences in (D) are instead denoted by asterisks (*). not shown). PAR and fow did not deviate signifcantly over time (p > 0.10) and remained close to their target values (see details in “Methods”). Although all fragments in the three culture systems were mushroom-shaped (Fig. 1B–D), many sof coral fragments cultured in the RAS−B system appeared unhealthy (Fig. 1B); polyps were not always extended, and neither their buoyant weight [BW; Fig. 2A; one-way ANOVA efect of time (for this and all following tests in this paragraph), F = 1.77, p = 0.134] nor their ODD (Fig. 2B; F = 0.0629, p = 0.8023) increased signifcantly over time. Tey also paled signifcantly over this period when pooling across all light × fow treatments (Fig. 2C; F = 53.1, p < 0.0001), though the color decrease of RAS−B corals of the two low-light treatments [high-light + low fow (Fig. 2D-1) and high-light + high fow (Fig. 2D-2)] was not statistically signif- cant. Afer changing to the RAS+B system (see Fig. 1C for representative fragment images.), their ODD enlarged (Fig. 2B; F = 9.54, p < 0.01), and their pigmentation increased (Fig. 2C; F = 32.8, p < 0.0001). Green, flamentous | (2020) 10:20200 | Vol.:(0123456789) www.nature.com/scientificreports/ Figure 3. Principal components analysis of correlations across standardized sof coral physiological response variable data. Please note that specifc growth rate (SGR), color change, and oral disc diameter (ODD) all refect rates or changes over time (day−1, fnal–initial, and % change day−1, respectively); fnal values were instead incorporated for percent (%) organic weight (i.e., AFDW), which was only measured once. Tere was a clear inverse relationship between % ODD change day-1 and AFDW. algae tended to overgrow the pedestals in the FTS (Fig. 1D), and neither buoyant weight (Fig. 2A; p = 0.635) nor ODD (Fig. 2B; p = 0.120) increased signifcantly between culture days 110 and 170. FTS fragment color actually decreased over this same period (Fig. 2C), though the global temporal diference was not statistically signifcant (p = 0.204; see also Fig.
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